The Neuro- of Cerebrovascular Disease*

JOHN W. HARBISON, M.D.

Associate Professor, Department of Neurology, Medical College of Virginia, Health Sciences Division of Virginia Commonwealth University, Richmond

The neuro-ophthalmology of cerebrovascular however, are important pieces to the puzzle the disease is a vast plain of neuro-ophthalmic vistas, patient may present. A wide variety of afflictions encompassing virtually all areas of disturbances of of the occur by virtue of its arterial dependence the eye-brain mechanism. This paper will be re­ on the internal carotid artery. It is also logical to stricted to those areas of the neuro-ophthalmology assume that changes in the distribution of the of cerebrovascular disease which one might con­ ophthalmic artery may reflect changes taking place sider advances in its clinical diagnosis and treatment. in other channels of the internal carotid artery­ Most practitioners of medical and surgical neu­ the middle cerebral, the anterior cerebral, and de­ rology give little thought to that aspect of medicine pending upon anatomic variations, the posterior generally accepted as the ideal approach to any cerebral artery. This paper will discuss these afflic­ disease-prevention. Usually when one is presented tions, those common as well as rare, those well with an illness of the central nervous system, it recognized, and those frequently overlooked. seems to be a fait accompli. Although prevention Historically, the recognition of the eye as an is by no means new, certain aspects of it qualify index of cerebrovascular disease presents an inter­ as advances. There is one advance in cerebrovascu­ rupted course. Virchow is credited with the first lar disease in which prevention plays a significant autopsy correlation of ipsilateral blindness with role. This is the recognition and surgical correction carotid thrombosis; Gowers in 1875 demonstrated of atherosclerotic lesions of the extracranial carotid embolization as a source of central retinal artery system which threaten the patient with that bane and middle cerebral artery occlusion, resulting in of antiquity-the "." monocular blindness and contralateral hemiplegia; Neuro-ophthalmology, largely by virtue of the Chiari followed in 1905 with his identification of carotid origin of the ophthalmic artery, plays a the carotid bifurcation as a common source of valuable role in the recognition, evaluation, therapy, atheromatous emboli to the cerebral circulation; in and prognosis of disease of the extracranial internal 1914 Ramsey Hunt emphasized the significance of carotid artery. Even this markedly restricted aspect transient symptoms involving the ipsilateral eye and of the neuro-ophthalmology of cerebrovascular dis­ contralateral extremities as strong evidence of ease is far too extensive to review adequately in . Thus by the turn of the century, the this paper. I have therefore selected for discussion stage was set for incrimination of the extracranial certain aspects of our neuro-ophthalmic approach internal carotid artery as a major source of "." to extracranial carotid disease. Some of these are Embolization was known as a basis for ipsilateral well known; others are less obvious and frequently eye and contralateral extremity symptoms and overlooked in our evaluation of patients. They all, signs; the carotid bifurcation was known as a source of emboli; and transient symptoms were recognized * Presented by Dr. Harbison at the 27th Annual as reflections of ischemia-a stroke prodrome or Stoneburner Lecture Series, February 7, 1974, at the Medi­ warning was discovered. Yet it was for Fisher in cal College of Virginia, Richmond. 1951 to rekindle interest in extracranial carotid

114 MCV QUARTERLY 10(3): 114-117, 1974 HARBISON: NEURO-OPHTHALMOLOGY OF CEREBROVASCULAR DISEASE 115

disease with his emphasis on transient ipsilateral one and one-half to two or three minutes despite visual and contralateral extremity symptoms as pre­ the patient's initial claim of five, ten minutes, or cursors of future strokes. It is this reawakening longer of impairment. A watch second hand or stop which has led directly to the current advances in watch could also be used; however, the vocal metro­ the medical and surgical neurologic care of extra­ nome seems helpful. cranial internal carotid disease. Although emphasis has been placed on the Amaurosis fugax, "fleeting blindness," has be­ association of ipsilateral eye and contralateral ex­ come a household phrase of those involved in the tremity , it should be recognized diagnosis and care of patients with carotid disease. that their actual temporal association is unnecessary The clinical picture of amaurosis fugax is reasonably diagnostically and infrequent clinically. The eye straightforward. It consists of transient monocular symptoms and signs in isolation as evidence of painless visual loss. Much has been made of the cervical internal carotid disease are, in all likelihood, character, duration, mode of onset, and resolution far more common than many practitioners realize. of the visual loss. Perhaps too much emphasis has The work of Lubow and associates at Ohio State been placed on such characteristic patterns as the regarding "retinal strokes" underlines this concept. window shade or picket fence effect. As a result, On rare occasions, transient homonymous visual we find that many patients we see have already been impairment may be a reflection of internal carotid "well educated" by housestaff. The potential patterns disease by virtue of a carotid origin of the posterior of visual loss are many. They include 1) an upper cerebral artery. Correct diagnosis will depend upon altitudinal loss of vision, "the window shade"; 2) a associated symptoms and signs. lower altitudinal loss of vision, "the picket fence"; The precise pathophysiology of these brief 3) a generalized peripheral loss of vision; 4) a total alterations of visual function continues to excite blackout of vision; and 5) a central blurring of some debate. It seems certain that most are based vision. The onset is most frequently abrupt; the upon emboli of either platelet aggregates or athero­ curtain seldom drops or rises slowly. Occasionally, sclerotic debris. The exact point at which the em­ the event is associated with photopsia-crude visual bolus works its evil is less certain. As will be , usually in the form of showers or discussed, visible emboli in central retinal arterioles flecks of light but suggestions of geometric character must play a role; whether they are the sole inciting will sometimes be seen. The key factors differentiat­ force is less certain. Emboli to the choroid, not ing this photopsia from occipital disease and mi­ apparent clinically, may be important. The role of graine are its clear unilaterality, the patient's age, dynamic reduction of blood flow in the production and a detailed analysis of the history, which excludes of visual symptoms of carotid disease is probably as a consideration and supports amaurosis small. It does, however, in selected but infrequent fugax. The event need not be simply a blackout; instances, probably play a significant role. Total dimming with a sensation of color may occur with carotid occlusions obviously cause some transient green and yellow having popularity. In my experi­ visual symptoms; generally, the symptoms cease ences, color sensation has been uncommon. following the stabilization occurring postocclusiori. The duration is generally brief, lasting two Our diagnostic evaluation of patients with or three minutes, or rarely, five-to-ten minutes. We symptoms of transient visual loss consists of the have found a common tendency for patients to careful analysis and integration of the specific physi­ misjudge the time sequence with frequent exaggera­ cal signs with the presenting and elicited symptoms. tion of the period of visual loss. As this tendency Although we have defined amaurosis fugax as to misjudge the duration of visual handicap may transient painless monocular visual loss, occasionally, be bothersome diagnostically, we have adopted a residual deficits of vision remain. In addition, a simple time confirmation method. It consists of number of patients with cervical internal carotid instructing the patient that you are going to begin to disease present not with transient ipsilateral eye count and he is to assume that this is the onset symptoms but with fixed deficits. of his visual symptomatology. We encourage the Needless to say, the diagnostic evaluation of patient to "relive" the experience and with the use all patients with eye symptoms and signs suggesting of our verbal clock, determine the average duration ipsilateral carotid disease must begin with docu­ of visual loss. The rule is to find a duration of from mentation of visual function-this includes best 116 HARBISON: NEURO-OPHTHALMOLOGY OF CEREBROVASCULAR DISEASE corrected visual acuity, pupillary reactivity, and tery. Ophthalmodynamometry plays a definite, quantitative evaluation. Although we though limited, role in the diagnosis of atheroscle­ palpate neck vessels, much less than total absence rotic cervical internal carotid disease. With the value of vessel pulsation is lightly regarded. Auscultation of ODM's in perspective, we continue to use them is considered an important adjunct, with realiza­ routinely. tion that bruits at sites other than the suspected A discussion of amaurosis fugax is not com­ symptomatic area may be significant. A bruit in plete without a brief review of the differential diag­ isolation, however, is of dubious benefit. nosis. Although almost all transient monocular visual The final, but perhaps most valuable, aspect loss is due to internal carotid arterial disease, there of the neuro-ophthalmic diagnostic evaluation of are other considerations which include temporal patients suspected of harboring atherosclerotic dis­ arteritis, migraine and migraine equivalents, glau­ ease is the dilated funduscopic examination with the coma, papilledema, Raynaud's disease, and other recording of retinal artery pressures. If one is for­ emboli. It is seldom difficult to identify these addi­ tunate enough to be present during an amaurotic tional sources of transient monocular visual loss event, funduscopy may reveal white platelet emboli or if they are appropriately sought. bright cholesterol plaques passing through the central Amaurosis fugax, although the hallmark of retinal arterioles. As this is a distinctly uncommon occlusive internal carotid disease and certainly its opportunity, one must usually be satisfied with resi­ most common symptomatic neuro-ophthalmic pre­ due which remains behind-most commonly, bright sentation, is by no means the only eye manifesta­ cholesterol material lodged at arteriole bifurcations. tion encountered in internal carotid vascular disease. Hollenhorst, who first recognized the significance of The following discussion will describe a number of retinal emboii in 1961, recorded a 33% incidence of less commonly recognized clinical syndromes caused these "Hollenhorst plaques" in patients with sympto­ by occlusive internal carotid disease. matic cerebrovascular insufficiency. Retinal stroke, although commonly an integral Ophthalmodynamometry (ODM) should be aspect of the syndrome of amaurosis fugax, cer­ routinely performed following a thorough fundu­ tainly occurs in the absence of prior symptomatic scopic survey. The technique of ODM was first transient monocular visual loss; there can be little devised by Baillart in 1917 to measure central doubt that the occurrence strongly suggests athero­ artery pressure. Svien and Hollenhorst popularized sclerotic disease of the cervical internal carotid its use in 1956. One must keep in mind that ODM's artery. The work of Lubow and associates at Ohio are not a measurement of absolute pressures. This State in 1972 has shown, angiographically, a 95% is, by and large, not a disadvantage as their primary incidence of carotid bifurcation disease in patients benefit is a relative comparison of one eye with having retinal strokes as compared to asymptomatic the other. We, as do many others, commonly record age-matched controls in which angiography demon­ only the diastolic reading and routinely perform strated a 25 % incidence of bifurcation abnormal­ the ODM's in the sitting position. Before we con­ ities. What do re.tinal strokes consist of? They sider the asymmetry significant, we require a 15 % consist of occlusive disease of the , previously difference when the readings are below 40 units and relegated to ophthalmic practice. It has become ap­ a 20% difference when the readings are above 40 parent, however, that many "retinal strokes" are units. Any readings below 20 units are considered of embolic origin and manifest cholesterol plaques abnormal. The basic mechanism of ODM is the exactly like those seen in amaurosis fugax. simple increase of intraocular pressure to levels Central retinal artery and artery branch oc­ above the central artery pressure. Needless to say, clusions, as well as more distal cholesterol emboli, either increased or decreased intraocular tension producing peripheral defects frequently unappreci­ will falsely alter the reading obtained. For this ated by the patient, constitute the retinal stroke. reason, tonometry-the recording of intraocular Their clinical manifestation is abrupt, usually ­ pressure-is essential in conjunction with ophthal­ less, persistent monocular visual loss. Blindness and modynamometry. Despite great care in technique, optic atrophy frequently follow retinal strokes. In false negative readings abound. Our experience has our brief historical review, one may recall Gowers' suggested that significant ophthalmodynamometric allusion to ipsilateral optic atrophy and blindness as­ asymmetry indicates extreme stenosis, if not actual sociated with contralateral hemiplegia. Carotid dis­ occlusion, of the symptomatic internal carotid ar- ease is obviously likely with this association. What HARBISON: NEURO-OPHTHALMOLOGY OF CEREBROVASCULAR DISEASE 117 must not be forgotten is that isolated blindness and iris. This will often culminate in occlusion of the optic atrophy may also reflect cervical internal ca­ anterior chamber angle and a malignant form of rotid disease. Other funduscopic alterations causally secondary glaucoma referred to as neovascular or related to cervical or extracranial internal carotid hemorrhagic glaucoma. disease occur. It is not commonly recognized that It is obvious that the last three syndromes ipsilateral carotid occlusive disease may serve to pre­ reflecting eye involvement, secondary not simply vent the expression of both hypertensive and diabetic to carotid stenosis but most certainly to more severe retinopathy. When a patient is seen with remarkably carotid occlusive disease, as well as occlusive disease asymmetric hypertensive or diabetic retinopathy, con­ of the usual orbital collateral channels, may occur sideration of the possible presence of occlusive in­ either in sequence or in combination. Their inci­ ternal carotid disease should follow. dence in reality is quite low. Ischemic retinopathy, Ischemic retinopathy, recognized as evidence a less severe manifestation of the same process, is of chronic retinal ischemia by Kearns and Hollen­ reported in only 5 % of unilateral carotid occlusions. horst in 1963, is a syndrome consisting of a retinal It is wise, however, to realize that eye signs other picture similar to diabetic retinopathy with dilated than simple transient or permanent monocular visual veins, some resultant blot hemorrhages and micro­ loss may point to disease of the cervical carotid aneurysms, low ophthalmodynamometric values, and vessels. at times, severe orbital pain. Ischemic retinopathy In conclusion, one should mention the occur­ can be differentiated from diabetic retinopathy by the rence of unilateral Homer's syndrome in a not fact that it is unilateral and that there is no biochemi­ insignificant number of unilateral internal carotid cal evidence of diabetes mellitus. Obviously, diabetes occlusions. This quite likely represents involvement and the Kearns ischemic retinopathy may coexist. by edema and ischemia of the carotid sympathetic The significance of ischemic retinopathy is its re­ plexus in the adventitia. flection of severe impairment of internal carotid as well as collateral circulation to the eye and BIBLIOGRAPHY orbit. Not uncommonly, the major trunks from the aortic arch are the site of the vascular occlusion. ALLEN N , MUSTIAN V : Origin and significance of vascular There are three additional presentations of murmurs of the head and neck. Medicine 41:227, 1962. eye signs reflecting occlusive vascular disease which DAVID JE, HUMPHRIES AW, YOUNG JR, BEVEN EG: A generally indicate, as does ischemic retinopathy, a correlation of neck bruits and atherosclerotic carotid ar­ more severe and diffuse vascular embarrassment of teries. Arch Surg 107 :729, 1973 . orbital as well as central retinal circulation. 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